title: Electronic structure of six-coordinate iron(III)-porphyrin NO adducts: the elusive iron(III)-NO(radical) state and its influence on the properties of these complexes.
abstract: This paper investigates the interaction between five-coordinate ferric hemes with bound axial imidazole ligands and nitric oxide (NO). The corresponding model complex, [Fe(TPP)(MI)(NO)](BF4) (MI = 1-methylimidazole), is studied using vibrational spectroscopy coupled to normal coordinate analysis and density functional theory (DFT) calculations. In particular, nuclear resonance vibrational spectroscopy is used to identify the Fe-N(O) stretching vibration. The results reveal the usual Fe(II)-NO(+) ground state for this complex, which is characterized by strong Fe-NO and N-O bonds, with Fe-NO and N-O force constants of 3.92 and 15.18 mdyn/A, respectively. This is related to two strong pi back-bonds between Fe(II) and NO(+). The alternative ground state, low-spin Fe(III)-NO(radical) (S = 0), is then investigated. DFT calculations show that this state exists as a stable minimum at a surprisingly low energy of only approximately 1-3 kcal/mol above the Fe(II)-NO(+) ground state. In addition, the Fe(II)-NO(+) potential energy surface (PES) crosses the low-spin Fe(III)-NO(radical) energy surface at a very small elongation (only 0.05-0.1 A) of the Fe-NO bond from the equilibrium distance. This implies that ferric heme nitrosyls with the latter ground state might exist, particularly with axial thiolate (cysteinate) coordination as observed in P450-type enzymes. Importantly, the low-spin Fe(III)-NO(radical) state has very different properties than the Fe(II)-NO(+) state. Specifically, the Fe-NO and N-O bonds are distinctively weaker, showing Fe-NO and N-O force constants of only 2.26 and 13.72 mdyn/A, respectively. The PES calculations further reveal that the thermodynamic weakness of the Fe-NO bond in ferric heme nitrosyls is an intrinsic feature that relates to the properties of the high-spin Fe(III)-NO(radical) (S = 2) state that appears at low energy and is dissociative with respect to the Fe-NO bond. Altogether, release of NO from a six-coordinate ferric heme nitrosyl requires the system to pass through at least three different electronic states, a process that is remarkably complex and also unprecedented for transition-metal nitrosyls. These findings have implications not only for heme nitrosyls but also for group-8 transition-metal(III) nitrosyls in general.
authors.affiliation: Department of Chemistry, University of Michigan, Ann Arbor, Michigan 48109, USA.
authors.forename: V K K
authors.initials: VK
authors.lastname: Praneeth
authors.forename: Florian
authors.initials: F
authors.lastname: Paulat
authors.forename: Timothy C
authors.initials: TC
authors.lastname: Berto
authors.forename: Serena DeBeer
authors.initials: SD
authors.lastname: George
authors.forename: Christian
authors.initials: C
authors.lastname: Näther
authors.forename: Corinne D
authors.initials: CD
authors.lastname: Sulok
authors.forename: Nicolai
authors.initials: N
authors.lastname: Lehnert
mesh_terms: D018360:Crystallography, X-Ray; D004583:Electrons; D005296:Ferrous Compounds / Q000737:chemistry*; D006418:Heme / Q000737:chemistry; D007501:Iron / Q000737:chemistry*; D008958:Models, Molecular; D015394:Molecular Structure; D009569:Nitric Oxide / Q000737:chemistry*; D011166:Porphyrins / Q000737:chemistry*; D013055:Spectrophotometry, Infrared; D014732:Vibration
chemical_list: D005296:Ferrous Compounds; D011166:Porphyrins; D009569:Nitric Oxide; D006418:Heme; D007501:Iron